Serotonergic modulation of local network processing in V1 mirrors previously reported signatures of local network modulation by spatial attention
Language English Country France Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't, Research Support, N.I.H., Intramural
Grant support
ZIA EY000570
Intramural NIH HHS - United States
PubMed
36878879
PubMed Central
PMC11610500
DOI
10.1111/ejn.15953
Knihovny.cz E-resources
- Keywords
- awake behaving macaque, behavioural state, local field potential, neuromodulation, primary visual cortex, serotonin,
- MeSH
- Action Potentials physiology MeSH
- Humans MeSH
- Macaca mulatta MeSH
- Serotonin MeSH
- Photic Stimulation MeSH
- Visual Perception physiology MeSH
- Evoked Potentials, Visual * MeSH
- Visual Cortex * physiology MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, N.I.H., Intramural MeSH
- Names of Substances
- Serotonin MeSH
Sensory processing is influenced by neuromodulators such as serotonin, thought to relay behavioural state. Recent work has shown that the modulatory effect of serotonin itself differs with the animal's behavioural state. In primates, including humans, the serotonin system is anatomically important in the primary visual cortex (V1). We previously reported that in awake fixating macaques, serotonin reduces the spiking activity by decreasing response gain in V1. But the effect of serotonin on the local network is unknown. Here, we simultaneously recorded single-unit activity and local field potentials (LFPs) while iontophoretically applying serotonin in V1 of alert monkeys fixating on a video screen for juice rewards. The reduction in spiking response we observed previously is the opposite of the known increase of spiking activity with spatial attention. Conversely, in the local network (LFP), the application of serotonin resulted in changes mirroring the local network effects of previous reports in macaques directing spatial attention to the receptive field. It reduced the LFP power and the spike-field coherence, and the LFP became less predictive of spiking activity, consistent with reduced functional connectivity. We speculate that together, these effects may reflect the sensory side of a serotonergic contribution to quiet vigilance: The lower gain reduces the salience of stimuli to suppress an orienting reflex to novel stimuli, whereas at the network level, visual processing is in a state comparable to that of spatial attention.
Department of Physiology 3rd Faculty of Medicine Charles University Prague Czech Republic
Werner Reichardt Centre for Integrative Neuroscience University of Tübingen Tübingen Germany
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Azimi Z, Barzan R, Spoida K, Surdin T, Wollenweber P, Mark MD, Herlitze S, Jancke D (2020) Separable gain control of ongoing and evoked activity in the visual cortex by serotonergic input. Elife 9:e53552. PubMed PMC
Banaie Boroujeni K, Tiesinga P, Womelsdorf T (2020) Adaptive spike-artifact removal from local field potentials uncovers prominent beta and gamma band neuronal synchronization. J Neurosci Methods 330:108485. PubMed PMC
Bastos AM, Schoffelen J-M (2015) A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Front Syst Neurosci 9:175. PubMed PMC
Beliveau V, Ganz M, Feng L, Ozenne B, Højgaard L, Fisher PM, Svarer C, Greve DN, Knudsen GM (2017) A high-resolution in vivo atlas of the human brain’s serotonin system. J Neurosci 37:120–128. PubMed PMC
Berens P (2009) CircStat: A MATLAB Toolbox for Circular Statistics. J Stat Softw 31:1–21.
Berens P et al. (2018) Community-based benchmarking improves spike rate inference from two-photon calcium imaging data. PLoS Comput Biol 14:e1006157. PubMed PMC
Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP (2010) Chronux: a platform for analyzing neural signals. J Neurosci Methods 192:146–151. PubMed PMC
Brainard DH (1997) The Psychophysics Toolbox. Spat Vis 10:433–436. PubMed
Carhart-Harris RL et al. (2016) Neural correlates of the LSD experience revealed by multimodal neuroimaging. Proc Natl Acad Sci U S A 113:4853–4858. PubMed PMC
Chalk M, Herrero JL, Gieselmann MA, Delicato LS, Gotthardt S, Thiele A (2010) Attention reduces stimulus-driven gamma frequency oscillations and spike field coherence in V1. Neuron 66:114–125. PubMed PMC
Chandran KS S, Mishra A, Shirhatti V, Ray S (2016) Comparison of Matching Pursuit Algorithm with Other Signal Processing Techniques for Computation of the Time-Frequency Power Spectrum of Brain Signals. J Neurosci 36:3399–3408. PubMed PMC
Clarke HF, Walker SC, Crofts HS, Dalley JW, Robbins TW, Roberts AC (2005) Prefrontal serotonin depletion affects reversal learning but not attentional set shifting. J Neurosci 25:532–538. PubMed PMC
Cohen JY, Amoroso MW, Uchida N (2015) Serotonergic neurons signal reward and punishment on multiple timescales. Elife 4:e06346. PubMed PMC
Cohen MR, Maunsell JHR (2009) Attention improves performance primarily by reducing interneuronal correlations. Nat Neurosci 12:1594–1600. PubMed PMC
Correia PA, Lottem E, Banerjee D, Machado AS, Carey MR, Mainen ZF (2017) Transient inhibition and long-term facilitation of locomotion by phasic optogenetic activation of serotonin neurons. Elife 6:e20975. PubMed PMC
Das A, Ray S (2018) Effect of stimulus contrast and visual attention on spike-gamma phase relationship in macaque primary visual cortex. Front Comput Neurosci 12:66. PubMed PMC
Davis M, Strachan DI, Kass E (1980) Excitatory and Inhibitory Effects of Serotonin on Sensorimotor Reactivity Measured with Acoustic Startle. Science 209:521–523. PubMed
Dayan P (2012) Twenty-five lessons from computational neuromodulation. Neuron 76:240–256. PubMed
De Luna P, Veit J, Rainer G (2017) Basal forebrain activation enhances between-trial reliability of low-frequency local field potentials (LFP) and spiking activity in tree shrew primary visual cortex (V1). Brain Struct Funct 222:4239–4252. PubMed
Disney AA (2021) Neuromodulatory Control of Early Visual Processing in Macaque. Annu Rev Vis Sci 7:181–199. PubMed
Eastman KM, Huk AC (2012) PLDAPS: A hardware architecture and software toolbox for neurophysiology requiring complex visual stimuli and online behavioral control. Front Neuroinform 6:1. PubMed PMC
Fanselow MS, Lester LS (1988) A functional behavioristic approach to aversively motivated behavior: Predatory imminence as a determinant of the topography of defensive behavior. In: Evolution and learning (Bolles RC, ed), pp 185–212. Hillsdale, NJ, US: Lawrence Erlbaum Associates, Inc.
Flavell SW, Gogolla N, Lovett-Barron M, Zelikowsky M (2022) The emergence and influence of internal states. Neuron Available at: 10.1016/j.neuron.2022.04.030. PubMed DOI PMC
Flavell SW, Pokala N, Macosko EZ, Albrecht DR, Larsch J, Bargmann CI (2013) Serotonin and the neuropeptide PDF initiate and extend opposing behavioral states in C. elegans. Cell 154:1023–1035. PubMed PMC
Fonseca MS, Murakami M, Mainen ZF (2015) Activation of dorsal raphe serotonergic neurons promotes waiting but is not reinforcing. Curr Biol 25:306–315. PubMed
Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention. Science 291:1560–1563. PubMed
Fries P, Womelsdorf T, Oostenveld R, Desimone R (2008) The effects of visual stimulation and selective visual attention on rhythmic neuronal synchronization in macaque area V4. J Neurosci 28:4823–4835. PubMed PMC
Goard M, Dan Y (2009) Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12:1444–1449. PubMed PMC
Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A 86:1698–1702. PubMed PMC
Gregoriou GG, Gotts SJ, Zhou H, Desimone R (2009) High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324:1207–1210. PubMed PMC
Grossman CD, Bari BA, Cohen JY (2022) Serotonin neurons modulate learning rate through uncertainty. Curr Biol 32:586–599.e7. PubMed PMC
Haenny PE, Schiller PH (1988) State dependent activity in monkey visual cortex. Experimental Brain Research 69:225–244. PubMed
Herrero JL, Gieselmann MA, Sanayei M, Thiele A (2013) Attention-induced variance and noise correlation reduction in macaque V1 is mediated by NMDA receptors. Neuron 78:729–739. PubMed PMC
Jacob SN, Nienborg H (2018) Monoaminergic Neuromodulation of Sensory Processing. Front Neural Circuits 12:51. PubMed PMC
Katzner S, Nauhaus I, Benucci A, Bonin V, Ringach DL, Carandini M (2009) Local origin of field potentials in visual cortex. Neuron 61:35–41. PubMed PMC
Kjaerby C, Athilingam J, Robinson SE, Iafrati J, Sohal VS (2016) Serotonin 1B Receptors Regulate Prefrontal Function by Gating Callosal and Hippocampal Inputs. Cell Rep 17:2882–2890. PubMed PMC
Kleiner M, Brainard D, Pelli D, Ingling A, Murray R, Broussard C, Others (2007) What’s new in psychtoolbox-3? Perception 36:1.
Kometer M, Schmidt A, Jäncke L, Vollenweider FX (2013) Activation of serotonin 2A receptors underlies the psilocybin-induced effects on α oscillations, N170 visual-evoked potentials, and visual hallucinations. J Neurosci 33:10544–10551. PubMed PMC
Kosofsky BE, Molliver ME, Morrison JH, Foote SL (1984) The serotonin and norepinephrine innervation of primary visual cortex in the cynomolgus monkey (Macaca fascicularis). J Comp Neurol 230:168–178. PubMed
Krueger J, Disney AA (2019) Structure and function of dual-source cholinergic modulation in early vision. Journal of Comparative Neurology 527:738–750. PubMed PMC
Lepage KQ, Kramer MA, Eden UT (2011) The dependence of spike field coherence on expected intensity. Neural Comput 23:2209–2241. PubMed
Lőrincz ML, Adamantidis AR (2017) Monoaminergic control of brain states and sensory processing: Existing knowledge and recent insights obtained with optogenetics. Progress in Neurobiology 151:237–253. PubMed
Lottem E, Banerjee D, Vertechi P, Sarra D, Lohuis MO, Mainen ZF (2018) Activation of serotonin neurons promotes active persistence in a probabilistic foraging task. Nat Commun 9:1000. PubMed PMC
Lottem E, Lörincz ML, Mainen ZF (2016) Optogenetic Activation of Dorsal Raphe Serotonin Neurons Rapidly Inhibits Spontaneous But Not Odor-Evoked Activity in Olfactory Cortex. J Neurosci 36:7–18. PubMed PMC
Mallat SG, Zhang Z (1993) Matching pursuits with time-frequency dictionaries. IEEE Trans Signal Process 41:3397–3415.
Marder E (2012) Neuromodulation of neuronal circuits: back to the future. Neuron 76:1–11. PubMed PMC
Marques JC, Li M, Schaak D, Robson DN, Li JM (2019) Internal state dynamics shape brainwide activity and foraging behaviour. Nature 577:239–243. PubMed
Matias S, Lottem E, Dugué GP, Mainen ZF (2017) Activity patterns of serotonin neurons underlying cognitive flexibility. Elife 6:e20552. PubMed PMC
Maya Vetencourt JF, Sale A, Viegi A, Baroncelli L, De Pasquale R, O’Leary OF, Castrén E, Maffei L (2008) The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 320:385–388. PubMed
Michaiel AM, Parker PRL, Niell CM (2019) A Hallucinogenic Serotonin-2A Receptor Agonist Reduces Visual Response Gain and Alters Temporal Dynamics in Mouse V1. Cell Rep 26:3475–3483.e4. PubMed PMC
Mitchell JF, Sundberg KA, Reynolds JH (2009) Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 63:879–888. PubMed PMC
Miyazaki KW, Miyazaki K, Tanaka KF, Yamanaka A, Takahashi A, Tabuchi S, Doya K (2014) Optogenetic activation of dorsal raphe serotonin neurons enhances patience for future rewards. Curr Biol 24:2033–2040. PubMed
Morrison JH, Foote SL (1986) Noradrenergic and serotoninergic innervation of cortical, thalamic, and tectal visual structures in Old and New World monkeys. J Comp Neurol 243:117–138. PubMed
Muthukumaraswamy SD, Carhart-Harris RL, Moran RJ, Brookes MJ, Williams TM, Errtizoe D, Sessa B, Papadopoulos A, Bolstridge M, Singh KD, Feilding A, Friston KJ, Nutt DJ (2013) Broadband cortical desynchronization underlies the human psychedelic state. J Neurosci 33:15171–15183. PubMed PMC
Nauhaus I, Busse L, Carandini M, Ringach DL (2009) Stimulus contrast modulates functional connectivity in visual cortex. Nat Neurosci 12:70–76. PubMed PMC
Nienborg H, Bridge H, Parker AJ, Cumming BG (2004) Receptive field size in V1 neurons limits acuity for perceiving disparity modulation. J Neurosci 24:2065–2076. PubMed PMC
Okun M, Steinmetz N, Cossell L, Iacaruso MF, Ko H, Barthó P, Moore T, Hofer SB, Mrsic-Flogel TD, Carandini M, Harris KD (2015) Diverse coupling of neurons to populations in sensory cortex. Nature 521:511–515. PubMed PMC
Pelli DG (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10:437–442. PubMed
Pinto L, Goard MJ, Estandian D, Xu M, Kwan AC, Lee S-H, Harrison TC, Feng G, Dan Y (2013) Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat Neurosci 16:1857–1863. PubMed PMC
Quinn KR, Seillier L, Butts DA, Nienborg H (2021) Decision-related feedback in visual cortex lacks spatial selectivity. Nat Commun 12:4473. PubMed PMC
Rasch MJ, Gretton A, Murayama Y, Maass W, Logothetis NK (2008) Inferring spike trains from local field potentials. J Neurophysiol 99:1461–1476. PubMed
Rauch A, Rainer G, Logothetis NK (2008) The effect of a serotonin-induced dissociation between spiking and perisynaptic activity on BOLD functional MRI. Proc Natl Acad Sci U S A 105:6759–6764. PubMed PMC
Ray S (2015) Challenges in the quantification and interpretation of spike-LFP relationships. Curr Opin Neurobiol 31:111–118. PubMed
Ray S, Hsiao SS, Crone NE, Franaszczuk PJ, Niebur E (2008) Effect of stimulus intensity on the spike-local field potential relationship in the secondary somatosensory cortex. J Neurosci 28:7334–7343. PubMed PMC
Ray S, Maunsell JHR (2011a) Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol 9:e1000610. PubMed PMC
Ray S, Maunsell JHR (2011b) Network rhythms influence the relationship between spike-triggered local field potential and functional connectivity. J Neurosci 31:12674–12682. PubMed PMC
Roelfsema PR, Lamme VAF, Spekreijse H (1998) Object-based attention in the primary visual cortex of the macaque monkey. Nature 395:376–381. PubMed
Seillier L, Lorenz C, Kawaguchi K, Ott T, Nieder A, Pourriahi P, Nienborg H (2017) Serotonin decreases the gain of visual responses in awake macaque V1. J Neurosci 37:11390–11405. PubMed PMC
Seo C, Guru A, Jin M, Ito B, Sleezer BJ, Ho Y-Y, Wang E, Boada C, Krupa NA, Kullakanda DS, Shen CX, Warden MR (2019) Intense threat switches dorsal raphe serotonin neurons to a paradoxical operational mode. Science 363:538–542. PubMed PMC
Spyropoulos G, Bosman CA, Fries P (2018) A theta rhythm in macaque visual cortex and its attentional modulation. Proc Natl Acad Sci U S A 115:E5614–E5623. PubMed PMC
Theis L, Berens P, Froudarakis E, Reimer J, Román Rosón M, Baden T, Euler T, Tolias AS, Bethge M (2016) Benchmarking spike rate inference in population calcium imaging. Neuron 90:471–482. PubMed PMC
Theis L, Chagas AM, Arnstein D, Schwarz C, Bethge M (2013) Beyond GLMs: a generative mixture modeling approach to neural system identification. PLoS Comput Biol 9:e1003356. PubMed PMC
Thiele A, Bellgrove MA (2018) Neuromodulation of Attention. Neuron 97:769–785. PubMed PMC
van der Meer MAA, Redish AD (2009) Low and high gamma oscillations in rat ventral striatum have distinct relationships to behavior, reward, and spiking activity on a learned spatial decision task. Front Integr Neurosci 3:9. PubMed PMC
Victoria Puig M, Watakabe A, Ushimaru M, Yamamori T, Kawaguchi Y (2010) Serotonin Modulates Fast-Spiking Interneuron and Synchronous Activity in the Rat Prefrontal Cortex through 5-HT1A and 5-HT2A Receptors. J Neurosci 30:2211–2222. PubMed PMC
Watakabe A, Komatsu Y, Sadakane O, Shimegi S, Takahata T, Higo N, Tochitani S, Hashikawa T, Naito T, Osaki H, Sakamoto H, Okamoto M, Ishikawa A, Hara S-I, Akasaki T, Sato H, Yamamori T (2009) Enriched expression of serotonin 1B and 2A receptor genes in macaque visual cortex and their bidirectional modulatory effects on neuronal responses. Cereb Cortex 19:1915–1928. PubMed PMC
Xing D, Yeh C-I, Shapley RM (2009) Spatial spread of the local field potential and its laminar variation in visual cortex. J Neurosci 29:11540–11549. PubMed PMC